food partitioning among malagasy primates

Oecologia (Berlin) (1988) 75:436-450 Oecologia �9 Spfinger-Verlag 1988

Food partitioning among Malagasy primates Jiirg U. Ganzhorn Abteilung Verhaltcnsphysiologie, Beim Kupferhammer 8, D-7400 Tiibingen, Federal Republic of Germany and Duke University Primate Center, Durham, NC 27705, USA

Summary. Food partitioning among lemurs was studied in relation to food patch size and plant chemistry in the eastern rainforest and a western deciduous forest of Madagas- car. Patch size (i.e. crown diameter of food trees) is significantly correlated with group body weight of different lemur species. But intraspecific variability is high and prevents effective species separation. Chemical analyses of more than 400 plant parts eaten by seven different lemur species re- vealed major differences in their food choice with respect to protein concentrations, condensed tannins and alkaloids. Among the leaf eating lemurs discriminant analysis segre- gates three groups A two species based on chemical characteristics of their food. Whereas differences in food chemistry are pronounced between groups they are lacking between the two species within each group. The two species of each group avoid interference competition by different activity rhythms. Actual competition for slowly renewable resources such as leaves and fruit, however, can not be reduced by different activities. Here interspecific differences in gross categories of food, food species composition and different habitat utilization due to other constraints may contribute to the possible coexistence of species. Thus interspecific differences in food selection in relation to primary and secondary plant chemicals is an integrated part of the mechanisms allowing several primate species to coexist in sympatry.

Key words: Lemur community - Food selection - Plant chemistry

The eastern rainforest of Madagascar houses one of the world's most diverse primate communities (Bourlirre 1985; Mittermeier and Oates 1985). However, little is known about the ecological mechanisms allowing a dozen or so lemur species to coexist in this environment today, not to mention the tremendously diverse community only a few hundred years ago (Dewar 1984).

In other tropical rainforests the coexistence of primate species can be linked to interspecific differences in habitat utilization, feeding habits or social organization. Specific adaptations for predator avoidance and feeding behaviour associated with these factors play the dominant roles struc- turing primate communities (Clutton-Brock and Harvey 1977; Wrangham 1980; Terborgh 1983; van Schaik and van Hooff 1983; Richard 1985; contr, to Smuts et al. 1986). The lemur community living in the eastern rainforest of

Madagascar deviates of what is known from other primate communities in two ways. First the diversity of social systems is rather limited compared to other regions. Second there seems to be large overlap in feeding habits, most species being either folivorous or mixed folivores-frugivores (Hladik 1979; Pollock 1979). According to the conventional wisdom, this reduced niche diversification might be caused by mitigated competition in an island situation combined with limited predation pressure. In fact, at least for the larger species, there seems to be no need for sophisticated anti-predator behaviour. Thus the fairly uniform social systems and the lack of large groups could well be linked to limited predation pressure. But the lack of differentiation with respect to feeding habits seems to violate Hutchinson's (1957) notion of the niche and of community organization.

Indeed, some arguments make it debatable to causally link coexistence of species to niche differentiation (for a discussion see contr, to Amer. Nat. 1983 Vol. 122(5)). If this is so - and up to now no rigorous experiment has been performed to test the role of competition for resource partitioning in primate communities - the coexistence of several sympatric folivorous species could well be interpreted as a product of chance alone. Nevertheless, based on Gause's experiments (reprinted 1969) I would like to adhere to the concept of Hutchinson's niche (1957) and consider interspecific differences in resource utilization as a major factor allowing coexistence. This notion is sup- ported by the conclusions reached by Terborgh (1986) that e.g. the Amazonian primate community of Cocha Cachu is food limited, facilitating the evolution of differential resource utilization. Additional support comes from studies of the large guild of African herbivores (reviewed by McNaughton and Georgiadis 1986). Here species-specific preferences for grass, browse and different plant parts (leaf, stem, sheet, etc.) also contribute to species separation. Whereas fruit provide ample opportunities for diversification based on physical as well as on chemical features (van Roosmalen 1984; Glaser and Hobi 1985; Sourd and Gau- tier-Hion 1986), the options for arboreal folivores with respect to leaves are restricted mainly to chemical characteristics. But except for the work of Hladik and his collaborators (Hladik et al. 1971 ; Hladik 1977) plant chemistry has been related only to food selection of single species in most pri- matological studies (reviewed by Glander 1982; Waterman 1984; Ganzhorn unpublished work).

In the study reported here it was tested whether or not plant chemistry does contribute to the separation of lemur

species in Madagascar. It will be shown that species separation of folivorous and frugivorous lemurs is in fact incom- plete only when "macroscopic" dietary features are considered. Niche diversification is apparent, however, when the chemical characteristics of the food are taken into account.

Methods

Study sites

The main study was carried out in the For& d'Analamazoa- tra near Andasib6 (Prrinet) from August to October 1984 and from September 1985 to February 1986. Andasib~ is located in the eastern rainforest of Madagascar. Detailed descriptions of the study site can be found in Pollock (1975a, b).

Two short observation periods (Dec. 12-16, 1985 and Jan. 3-9, 1986) were carried out in the For& de Ankarafant- sika at Ampijoroa, located in the western dry deciduous forest of Madagascar. The study site is described by Ri- chard (1978).

Observation methods

Lemurs were searched for by walking very slowly along a trail. Once an animal or a group of animals was found, it was watched and followed for as long as possible. All animals except the indris at Andasib~ were unhabituated and no attempt was made to follow them when they were fleeing. Observations were concentrated at the beginning and at the end of the day and of the night when the animals were most active. At Andasib6 some 450 h were spent in the forest at night, searching for and observing nocturnal lemurs. The amount of time spent in observations of and search for lemurs during the day was about the same. Beside the actual observation time, much time was spent collecting plant parts and describing the vegetation. Lemurs were followed whenever they were encountered during this kind of work. At Ampijoroa nocturnal census work and observations were carried out for about 40 h.

Estimation of primate population densities

Primate densities were estimated only for nocturnal species. For diurnal species population densities were calculated according to published data. Marked and mapped trails were censused repeatedly. Trail length was 3.2 km at Andasib6 and 1.7 km at Ampijoroa. Lateral visibility was about 5 m on each side of the trail at Andasib6 and 10 m at Ampi- joroa. Based on the length of the trails and the lateral visibility it was assumed that in each census an area of 3.2 km x 10 m=0.032 km 2 and 1.7 km x 20 m=0.034 km 2 were covered at Andasib+ and Ampijoroa respectively. Pri- mate densities were calculated for each census (25 at Anda- sibr, 10 at Ampijoroa). Normally the areas were censused twice in each census night. Animals located by sound but not seen were not included.

Feeding data

Feeding data of the following species were used in the analysis Andasib& Avahi 1. laniger, Cheirogaleus major, Hapale- tour griseus, [ndri indrL Lemur f fulvus, Lepilemur m. mustelinus, and Microeebus rufus; Ampijoroa: Avahi l. occidentalis and Lepilemur m. edwardsi. Except for H. griseus only

437

items from the same tree in which the animals had been found feeding were collected and analyzed. Feeding data on H. griseus were supplemented with data published by Pollock (1986) and provided by P.C. Wright (unpublished work). Therefore not all the individual plants H. griseus had been feeding on were known. Thus these results may not be comparable directly with the other lemur species.

For comparisons 45 different types of leaves of 32 individual trees were collected randomly at Andasib& In addi- tion leaves eaten were compared with other leaves that were not eaten but were available in the same tree simultaneous- ly.

Chemical analyses

At Andasib6 leaves of 163 species (273 different individual plants; 358 items) and pith, flowers and fruits of 52 species were analyzed qualitatively in triple assays for the presence of alkaloids with Mayer's, DragendorWs and Wagner's re- agent (Cromwell 1955). A plant part was considered to contain alkaloids when indicated by least two of the reagents. For the study presented here a subset of 219 dried leaf samples and 26 different dried fruits were ground to pass a 2 mm sieve. These samples were analyzed quantitatively for their concentrations of condensed (procyanidin) tannin (Oates et al. 1977; for an evaluation of the method see Mar- tin and Martin 1982; Mole and Waterman 1987a, b; Wisdom et al. 1987), extractable protein (with BioRad Pro- tein Assay, as equivalent of bovine serum albumin: Brad- ford 1976; extraction with 0.1 n NaOH: Eze and Dumbroff 1982), soluble sugar (as equivalent of galactose after acid hydrolyzation of 50% methanol extract: Kates 1972).

Fiber analyses were performed for a subset of the samples according to Goering and van Soest (1970). Neutral detergent fiber (NDF) represents the percentage of fiberous material non digestable by most herbivores. Acid detergent (ADF) is composed of cellulose and Iignin. Hemicellulose is given as the difference between NDF and ADF. This measurement represents a mixture of protein and carbohydrates. Negative values for hemicellulose can occur. In case the difference of NDF - ADF was negative, hemicellulose was assigned the value zero (the different methods of fiber analyses and some of the shortcomings are discussed by Robbins 1983).

The total amount of protein in leaves (determined with the Kjeldahl procedure) is comprised of the concentration of extractable protein plus the protein found in "hemicellulose". It can be calculated as: %Total protein= %extractable protein + 0.854 %hemicellulose- 5.09 (r = 0.854, P < 0.01, n = 10). Based on this relationship the concentration of total protein was calculated.

At Ampijoroa 22 leaf items eaten by A. laniger and L. mustelinus were analyzed for the components listed above.

Statistical analysis

Food items were not weighted by frequency of consumption for each lemur species. Instead each item was used only once in the interspecific comparison.

Statistical tests were performed according to Siegel (1956) and Miihleuberg (1976). Parametric tests were calculated after arcsine transformation of percentages. For mul- tivariate analysis SAS - programs were used (SAS 1985).

438

Table 1. The lemur community at Andasib6

Species Body weight Group size Population density Activity Diet Reference (kg) (No/km 2)

Avahi laniger 1.0 1-4 72 +_ 32 b nocturnal Leaves Cheirogaleus major 0.5 1-2 68 +_ 34 b nocturnal Flowers, Fruit, Leaves Hapalemur griseus 0.8 2-6 47 -62 diurnal Leaves (bamboo), Fruit 1, 2, 3 Indri indri 6-10 2-4 9 -- 16 diurnal Leaves, Fruit 1 Lemurfulvus 2-4 2-10 4 0 - 60 diurnal/nocturnal Fruit, Leaves 1 Lepilemur mustelinus 1.0 1-2 13 + 9 b nocturnal Leaves, Fruit, Flowers Microcebus rufus 0.06 1-2 110 • 34 b nocturnal Fruit, Insects Daubentonia madagascariensis a 3.0 1 nocturnal Insects, Fruit 4, 5, 6 Lemur rubriventer a 2-4 diurnal/nocturnal 1, 3 Propithecus diadema a 6.0 2-5 diurnal Fruit, Leaves 1, 3 Varecia variegata ~ 4.0 2-4 diurnal 1

Body weights are taken from Razanahoera - Rakotomalala (1981) and Tattersall (1982) a species present but not considered here b means and 95% confidence limits, based on 25 census walks along 3.2 km of marked and mapped trails 1 Pollock (1979), 2 Pollock (1986), 3 P.C. Wright (pers. comm.), 4 Petter and Peyrieras (1970), 5 Pollock et al. (1985), 6 Ganzhorn and Rabesoa (1986)

Table 2. The lemur community at Ampijoroa

Species Body weight Group size Population density Activity Diet Reference (kg) (Yo/km 2)

Avahi l. occidentalis 0.74.9 2-5 67 • 66 b nocturnal Leaves Cheirogaleus medius 0.3 1-2 81 + 368 nocturnal Flowers, Fruit Lemurf.fulvus 2--4 12 170 diurnal Fruit, Leaves 1 Lepilemur m. edwardsi 0.8-1 1-2 57 _+ 22 b nocturnal Leaves, Fruit Mierocebus murinus 0.06 1 42 • 19 b nocturnal Fruit, Insects Propitheeus verreauxi eoquereli 4 5 60 diurnal Fruit, Leaves, Flowers 2 Lemur mongoz a

Body weight are taken from Razanahoera - Rakotomalala (1981) and Tattersall (1982) a species found in the vicinity, but not present in the study area b means and 95% confidence limits, based on 10 census walks along 1.7 km of marked and mapped trails 1 Harrington (1975), 2 Richard (1978); population densities of the two diurnal species was calculated as mean group size x average home range

Results

Population densities

The number o f animals found varied greatly between months. A t Andasib6 for example, no C. major and L. mustelinus were seen in August and the beginning o f September. But up to 11 C. major were encountered in a single census in January. This could be due to the fact that June to Sep- tember are the coldest months o f the year at Andasib6 with mean minimal temperatures from 10.5 ~ C to 11.3 ~ C (mean o f 20 years f rom 1941-1960; Pol lock 1975 a).

Cheirogaleus sp., Microcebus sp. as well as Lepilemur sp. go into to rpor or at least reduce their activities during the coldest par ts o f the year which makes them difficult to detect (review in Tat tersal l 1982).

But, though the est imated popula t ion density of M. rufus was on the average 5 times lower in 1985/86 than in 1984 (Ganzhorn 1987b), the number o f sightings did not seem to depend on the t ime of the year (see also Mar t in 1972). Instead, the presence of M. rufus depended strongly on the availabil i ty o f fruiting scrubs and trees. After remov- ing all the fruiting scrubs (Clidemia hirta) along 500 m of a trail, the number o f M. rufus seen there on the average d ropped f rom 1.7 animals to 0 (P < 0.01; n l = 15; n2 = 10;

rtl, 2 = number of census walks before and after removal of the scrubs; median test).

Tota l biomass of lemurs in the eastern rainforest is a round 400 kg /km z (95% confidence limits: 237-635 kg/ km z, n = 25; Table 1). This estimate is within the range of pr imate biomass in different neotropical regions, but it is lower than estimates for t ropical rainforests in Afr ica and Asia (data compiled by Terborg and van Schaik, pers. comm.). At Ampi jo roa biomass is about 880 kg /km 2 (Ta- ble 2). This estimate is also lower than estimates of pr imate b iomass in another western forest of Madagasca r (Charles- Dominique et al. 1980). A possible reason for the low fig- ures could be that animals located only acoustically were not included in the census.

General feeding behavior

Most o f the species studied were feeding on leaves and fruits. F ru i t eating was negligible for A. laniger and H. griseus. M. rufus was seen only once nibbling on leaves.

Different lemur species in different sized groups tended to feed on trees of different crown diameters. Though cause and effect can not be teased apa r t in these post factum correlat ions, differences in crown sizes o f food trees can be interpreted to play a major role in reducing compet i t ion

between primate species in other areas of the world (Ter- 7 borgh and Janson 1986; Wright 1986). But they contribute little to species separation in Madagascar (Fig. 1). Crown ~. 6 diameters of food trees (y) can be related to the log of wc~ feeding group weights (x) with linear regression models (leaf w ~ 5 eating: y = 0 .77x- 3.18, r=0.44, N=226, P<0.001; fruit ~z

<s 4 eating: y=0.53x+0.09, r=0.47, N=125, P<0.001). 5 Though both models are highly significant they explain only ~ 3 some 19% and 22% of the variance in the utilization of o

t2~ food trees. Thus, taken alone, neither gross food categories u 2 nor tree size are sufficient to separate lemur species in Ma- dagascar.

Plant chemicals and lemur food selection

Comparisons between leaves eaten versus leaves not eaten, both growing on the same tree

There was no difference between preferred versus not preferred leaves with respect to carbohydrates. All species except L. mustelinus chose the item with the higher protein content. Once the animals were feeding in a particular tree, most of them did not discriminate against tannins. Only L. mustelinus chose the leaves with the lower tannin concentration (Table 3).

Interspecific comparisons of leaf selection by different lemur species at Andasibb

M. rufus was seen only once eating young leaves. Therefore this species is not considered in the following analysis. C. major frequently ate young leaves or leave buds of saplings. Often this kind of food source was depleted completely in one feeding bout. Thus, many food items of C. major which probably were rich in proteins but low in tannins could not be included in the analysis. Therefore the results of the chemical composition of leaves eaten by C. major might be distorted.

Means and standard deviations of different phytochemi- cals in leaves eaten by the different lemur species are listed in Table 4. Despite the uniform criteria underlying leaf selection of different lemur species once they have entered a given food tree (Table 3), there are major differences in the chemical composition of leaves eaten by the different species (Table 4). Using discriminant analysis (SAS 1985; Deichsel and Trampisch 1985) three pairs of species are distinguished among the leaf eating lemur species of Anda- sib& This separation is based on different reactions of the lemurs toward hemicellulose, extractable protein, condensed tannins and the presence of alkaloids. None of the other chemicals contributes to species separation once the effects of these chemicals have been accounted for. The classification summary of the discriminant analysis was transformed into the measurement of niche overlap (Cody 1974) or, rather, an index of similarity, as shown in Fig. 2. Differences between pairs are quite pronounced and highly significant. But leaf selection of the two species within a pair is either indistinguishable based on chemical characteristics (L indri and A. laniger) or only marginally significant.

Separation of species belonging to the same pair is achieved by some of the other factors mentioned above. Each pair consists of one diurnal and one nocturnal species, which can avoid immediate interference competition by different activity patterns (Charles-Dominique etal. 1980;

439

LEAF EATING

t

In GROUP BODY WEIGHT (g)

A I=

r'v' I L l I"-- LI.J y..

r-' l

Z 3= C ) r'r" I . j

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9-

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FRUIT EATING

0

o~ Ix DZ~

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z~

z~

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In GROUP BODY WEIGHT(g) Fig. 1. Relations between crown diameters of food trees and group body weight (given in log) of lemur species. Bars represent 95% confidence intervals, x =A. laniger; o=C. major; n=L indri; tx=L. fulvus; e=L. mustelinus; A=M. rufus

Wright 1985). Actual competition for slowly renewable resources such as leaves and fruit, however, can not be reduced by different activity rhythms. Here interspecific differences in gross categories of food composition and differential habitat utilization due to other constraints contribute to the possible coexistence of species.

Interspec~'c comparison of fruit selection by different lemur species at Andasibb

Only for C. major, L. fulvus and M. rufus enough different fruits were collected to allow statistical comparisons between the concentrations of different chemicals in their food (Table 5; Appendix 2). There was no difference between all three lemur species with respect to the concentrations of extractable protein and sugar. C. major and L. fulvus also did not react differently towards alkaloids and tannins. Fruits eaten by M. rufus had lower tannin concentrations than fruits eaten by either one of the other two species ( t= 3.626 and t= 3.617 respectively, P < 0.01).

440

Table 3. Comparison of the chemical composition of leaves eaten versus leaves not eaten, bo th growing on the same tree

Species Neutral Acid Hemicellulose Soluble sugar Total protein Extractable detergent detergent protein fiber fiber

Condensed tannin

A. laniger n = 1 4 n = l l n = 1 1 n = 1 4 n = l l n = 1 4 n = 1 4 T = 3 0 T = 4 0 T = 1 7 T = 5 3 T = 4** T = 8** T = 3 3

C. major n = 11 n.d. n.d. n = 11 n.d. n = 10 n = 11 T = 1 6 T = I 7 T = 5* T = 1 8

H. griseus not applicable

L indri n = 1 4 n = 1 0 n = 1 0 n = 1 9 n = 1 0 n = 1 9 n = 1 9 T = 5 8 T = 3 0 T = 1 6 T = 5 8 T = 1 3 T = I I * * T=99.5

L.fulvus n = 13 n.d. n.d. n = 13 n.d. n = 13 n = 13 T = 3 0 T = 1 8 T = 4** T = 2 7

L. mustelinus n = 13 n = 11 n = 11 n = 13 n = 11 n = 12 n = 13 T = 4 9 T = 1 7 T = 2 2 T = 1 9 T = 3 5 T=22.5 T = l l * *

n = number of comparisons; T = test statistic according to the Wilcoxon matched-pair signed-ranks test: * P < 0.05; ** P < 0.01

Table 4. Chemical composition of leaves eaten by different lemur species at Andasib& Except for condensed tannin and alkaloids values are means and standard deviations of concentrations in percentages. Condensed tannins are in relative units as equivalents of quebracho tannin. For alkaloids the percentage of items containing alkaloids is given. Statistics have been performed after arcsine transformation. The random sample was excluded for calculation of the unbalanced ANOVA at the end of the Table

Species Neutral Acid Hemicellulose Extractable Total Extractable Condensed Alkaloids detergent detergent sugar protein protein tannin fiber fiber

A. laniger 63.0 46.2 14.3 7.9 16.4 8.8 22.7 0 51.6-73.7 37.8-54.7 5.2-27,1 4.8-13.1 12.3-24.4 5.7-12.3 8.5-41.2 n = 3 6 n = 3 4 n = 1 8 n = 1 8 n = 3 4 n = 1 8 n = 3 4 n = 3 4

C. major 63.1 43.0 29.0 7.8 23,5 5.4 14.8 24 49.2-76.0 27.3 59.4 12.7-48.7 3.9-12.7 13.6-35.1 1.5-11.6 1.3-39.3 n=21 n = 1 8 n = 4 n = 4 n = 1 8 n = 4 n = 1 8 n - 1 8

H. griseus 70.4 29.7 39.1 10.0 22.5 3.5 2.8 0 54.5-84.2 22.3-37.7 29.5-49.1 4.8-16.7 15.3-30.7 1.8- 5.7 0.7- 6.5 n = 8 n = 8 n = 8 n = 8 n = 8 n = 2 n = 8 n 8

L indri 61.4 47.5 14.2 7.2 13.0 8.0 25.8 6 40.3-80.4 34.1~51.1 3.9-29.5 3.4-12.4 7.2-20.1 5.1-11.4 6.6-52.2 n = 3 4 n = 3 3 n = l l n = 1 1 n = 3 4 n = 1 1 n = 3 4 n = 3 4

L.fulvus 58.7 49.0 17.1 7.6 18.9 7.8 19.9 16 45.8-71.0 36.3 61.8 10.0-35.6 3.6-12.8 13.6-24.8 3.7-13.2 3.1-46.2 n = 3 1 n = 2 4 n = 3 n = 3 n = 2 5 n = 3 n = 2 5 n = 2 5

L. mustelinus 62.1 45.1 15.9 5.4 14.1 4.9 13.0 44 47.9-75.3 35.5 54.9 9.1-24.1 2.8- 8.8 8.4-20.9 1.3-10.6 2.9-28.7 n = 2 7 n = 2 5 n = 1 4 n = 1 4 n = 2 5 n = 1 4 n = 2 5 n = 2 5

Random sample 66.4 46.0 14.1 7.0 12.9 4.9 22.2 33 52.7-78.9 34.~58.1 6.2-24.4 4.2-10.5 6.9-20.5 1.8- 9.6 6.1-44.7 n = 4 5 n = 45 n = 20 n = 20 n = 45 n = 20 n = 45 n - 45

ANOVA (unbalanced)

F 1.04 3.82 5.47 1.87 1,79 5.13 3.95 df/Error 5/136 5/52 5/52 5/138 5/46 5/138 5/138 p 0.400 0.005 <0.001 0.104 0,134 <0.001 0.002 R 2 0.037 0.269 0.345 0.063 0,163 0.157 0.125

A l so n o n e o f t he 10 d i f f e ren t f ru i t s e a t en b y M. ru fus c o n t a i n e d a lka lo ids , w h e r e a s 4 o u t o f 12 a n d 5 o u t o f 21 d i f f e ren t f ru i t s c o n t a i n e d a lka lo ids for C. major a n d L. fuI- vus. H o w e v e r , due to sma l l s a m p l e size th is d i f fe rence be- t w e e n M. ru fus a n d the o t h e r two l e m u r species is n o t s ignif- i c a n t s ta t i s t ica l ly ( F i s h e r ' s exac t p r o b a b i l i t y tes t : P > 0.05).

Comparison AndasibO - Ampijoroa

Species c o m p o s i t i o n o f f ood p l a n t s e a t e n b y A. laniger a n d L. mustelinus was qu i t e d i f f e ren t b e t w e e n the two si tes (Ap- pend i ce s 1, 3). B u t in in t r a spec i f i c c o m p a r i s o n s n o difference was f o u n d b e t w e e n si tes c o n c e r n i n g the chemica l corn-

L E A F E A T I N G

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- - A.[aNger

L fulvus

L mustel inus

H griseus

Cmajor

D I F F E R E N C E S

between between species groups

H E * * *

ALK" ALK "** EP * EP H

s *"

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F R U I T E A T I N G

Lfulvus

C.rnajor

Hrufus

I I I i I [ I I i I

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N I C H E O V E R L A P

Fig. 2. Similarity of the chemical composition of leaves and fruit eaten by different lemur species at Andasib6. Best separation of species was determined with resubstitution models and tested with hold-out procedures in discriminant analyses (SAS 1985; Deichsel and Trampisch 1985). The classification summary was used to cal- culate an index of similarity between species (Cody 1974). Plant chemicals that contribute to species separation are listed: HC hemicellulose; EP extractable protein; CT condensed tannin; ALK alkaloids * P<0.05; ** P<0.01 ; *** P<0.00I

position of the diet of either species ( P > 0.05 for all chemicals). Nevertheless, species separation at Ampijoroa seems to follow the same principles as at Andasibr. At Ampijoroa A. laniger also selected leaves with higher concentrations of easily extractable protein than L. mustelinus. Also the former species discriminated against alkaloids, whereas the latter did not. Differences in tannin concentrations in the diet of the two species were also apparent, but they did not differ significantly due to large variation and small sample size (Table 6).

D i s c u s s i o n

Food resource partitioning among primates of the eastern Malagasy rainforest is achieved in a variety of different ways. There are differences in activity patterns, the relative importance of leaves in their diet and in food species composition (Tables 1, 2; Appendix). Furthermore there are marked differences in body weight, ranging from 60 g (3/. rufus) to about 6-10 kg (L indri). These differences are reflected in the utilization of different sized branches and other supports. Though at a restricted scope, compared to other primate communities, the social organization varies from mainly solitary species (M. rufus, C. major, L. mustelinus) to species living in family groups (indriids) and groups up to about 10 animals (L. fulvus) (Table 1). In general, individual body weight and "group body weight" are post-

Table 5. Chemical composition of fruits species at Andasib6

441

eaten by different lemur

Species Extractable Extractable Condensed Alkaloids sugar protein tannin

C. major 10.3 5.3 18.8 5.2-17.0 3.0- 8.2 3.6-41.9 33

n = t l n=l l n=11 n=12

L.fulvus 11.2 7.0 18.2 5.6--18.4 3.8-11.0 5.4-36.3 24

n=15 n=15 n=15 n=21

M. rufus 7.3 7.3 2.1 3.5-12.3 4.1-11.2 0.4- 5.2 0

n=7 n=7 n=7 n=10

ANOVA (unbalanced)

F 1.19 1.09 5.72 d f/Error 2/30 2/30 2/30 p 0.318 0.351 0.008 R 2 0.074 0.067 0.276

For details see Table 4

tively correlated with patch size, represented by the crown diameter of food trees (Fig. 1). There is also a clear vertical separation of species when feeding. All these factors contribute to niche separation of lemurs in the eastern rainforest of Madagascar. However, these distinctions are quite subtle and subject to variation. For example, L. fulvus, probaNy behaviorally the most flexible of the different lemur species, can be active at night as well as during the day. Also when feeding on young leaves the median of their group size is 2 (range 1-6; n = 18) but when eating fruits the median group size is 6 (range 2-20; n = 26), resem- bling the fission-fusion system of Ateles sp. or Pan troglo- dytes and providing an example of behavioral flexibility in relation to food patch size and food quality. Despite the statistically clear vertical separation of lemur species, each species can be found in any level of the forest. M. rufus, normally feeding in scrubs and little trees can also be seen in the top of the biggest trees. On the other hand, I. indri can feed on saplings within reach of the observer.

Parts of the different height preferences of lemurs can be explained by the vertical distribution of suitable sub- strates and the size of food patches. Large patches tend to occur in big trees high up in the canopy, small patches predominate in the undergrowth. But these preferences can not explain, how, for example, A. laniger is separated from L. fulvus. On the average, both species feed at about the same height in the same sized trees when they eat leaves. On the other hand, the two morphologically most similar species, A. laniger and L. mustelinus, are clearly distinct with respect to feeding height and crown diameters at An- dasib& But they are indistinguishable at Ampijoroa (Ganz- horn, in press),

It is here where the chemical composition of food plants might help in niche partitioning. In the examples mentioned above, all else being equal A. laniger include significantly fewer leaves with alkaloids in their diet than L. fulvus or than L. mustelinus in both areas. In general, all species, except L. mustelinus, seemed to follow the same rules when feeding. Given a choice in natural experiments (e.g. mature leaves - young leaves of the same tree), they select items with the higher concentration of easily extractable protein.

442

Table 6. Chemical composition of leaves eaten by A. laniger occidentalis and L. mustelinus edwardsi at Ampijoroa

Species Neutral Acid Hemicellulose Soluble Total Extractable detergent detergent sugar protein protein fiber fiber

Condensed Alkaloids tannin

A.I. occidentalis 63.5 44.9 16.7 7.2 18.4 8.6 25.7 55.6-71.1 2 9 . 6 - 6 0 . 8 5 . 8 - 3 1 . 8 3 . 4 - 1 2 . 2 9.4-29.6 5.8-12.0 3.2-59.7 0% n=10 n=9 n=9 n=9 n=9 n=10 n=9 n=11

L.m. edwardsi 64.1 40.8 20.5 7.1 16.1 4.5 15.2 53.2-74.3 28 .6 -53 .7 13 .9 -27 .9 4.6-10.1 9.7-23.9 2.2- 7.8 3.5-33.2 36% n=12 n-=13 n=12 n=12 n=12 n=13 n=13 n=14

Comparison of species F n.s. n.s. < 0.05 n.s. n.s. n.s. n.s. < 0.05 a t n.s. n.s. n.s. n.s. n.s. <0.01 n.s.

For explanations see Table 4 Fisher extract probability test

This result is consistent with the notion that primates eat leaves primarily for their proteins (Clutton-Brock and Harvey 1977; Hladik 1979). Since the amount of protein required to achieve balanced protein budgets scales to the 0.75 power of body weight (Robbins 1983), small animals need to select items with higher protein content. Though there is a close correlation between body weight and the total protein concentrations in leaves (Ganzhorn, unpubl. ms), total protein is of less importance for species separation than the content of extractable protein. Some species seem to rely more on easily extractable proteins, whereas other species select leaves where proteins are bound to the diverse fraction of "hemicellulose". Morphological differences such as the elongated small intestine of indriids, the enlarged caecum in L. mustelinus (Chivers and Hladik 1980; Hladik 1979) suitable for extensive microbial fermentation, or different dental structures in L. mustelinus and H. griseus (Seligson and Szalay 1978) can then be seen as adaptations to tap different sources of protein (via "hernicellulose": C. major, H. griseus; via easily extractable protein: A. laniger, L indri, or via microbial fermentation: L. mustelinus), resulting in effective food partitioning.

Secondary plant substances provide another level of species separation. The two indriids do not discriminate against tannins but avoid alkaloids. L. mustelinus does exactly the opposite (asking for reconsideration of the role the enlarged forestomach of colobines might have in community ecology), 1t. griseus avoids both, and the two other species do not discriminate with respect to these chemicals. Though yet untested these differences might reflect different abilities for detoxification (Brattsten 1979) or taste perception (Hla- dik 1979; Chapman and Blaney 1979; Glaser and Hobi 1985; Glaser 1986; Sourd and Gautier-Hion 1986; Ganz- horn 1987a, in press) thus paralleling interactions between plants and insects (Ehrlich and Raven 1964; Janzen and Waterman 1984; Rhoades 1985).

Up to this point it is not clear whether the observed preferences for specific plant chemicals reflect true choices or whether they represent mere correlations e.g. of habitat use. At Andasib~, L. mustelinus was feeding predominantly on leaves, growing in the lower levels of the forest. Since more woody plants of the understory contain alkaloids than plants of the canopy the preponderance of alkaloids in the diet of L. mustelinus might reflect indiscriminate leaf selection with respect to secondary components. The same could be true e.g. for the two indriids, A. laniger and L indri.

They were feeding higher up in the forest. There, alkaloids are rare but tannin levels tend to be quite high (Ganzhorn et al. unpublished work).

At Ampijoroa, however, A. laniger and L. mustelinus were feeding at the same height in the same sized trees. Here, some 300 km west of Andasib6, the chemical composition of leaves consumed by A. laniger and L. mustelinus was the same as at Andasib6. In both areas the two species differed significantly with respect to extractable protein and alkaloids (Tables 4, 6).

Thus different reactions towards plant chemicals do not represent just correlations of different habitat utilization by different species. Rather they might reflect species specific needs or abilities for detoxification or taste perception (see lit. cited above).

Conclusion

Primate communities are believed to be structured by interspecific feeding differences and behaviour to avoid preda- tors. These differences are reflected in different social orga- nizations linked to food patch size and different degrees of folivory and frugivory. In the supposedly relaxed com- petitive situation of Madagascar these differences appear not to exist, suggesting that the Hutchinsonian notion of niche diversification may not apply. However, if chemical differences in the composition of food plants are considered, the niches of the different species appear distinct. Thus, the island situation does not result in increased eclogi- cal overlap between species. Rather it necessitates new and more subtle mechanisms to achieve niche diversification.

Acknowledgements. I am grateful to the Minist6re des Eaux et For- &s, the Minist6re de l'Enseignement Sup~rieur, and the Duke Uni- versity Primate Center for their permission to work in Madagascar and for their logistic support. J.-P. Abraham identified the plants. E.M. Haydt and J. Rabesoa assisted in data collecting. J.I. Pollock, E.L. Simons and P.C. Wright provided logistic support and unpublished data on food plants of H. griseus. Chemical analyses could be carried out in the labs of the Landesanstalt ffir landwirtschaft- liche Chemic (Hohenheim) and of H.U. Seitz (Univ. Tfibingen). J. Dittami, P.H. Klopfer and J.I. Pollock made very helpful com- ments on the manuscript. A. Buschold, E.M. Haydt and C. Kunze helped greatly preparing the manuscript. In particular I would like to acknowledge the support of K. Schmidt-Koenig. The study was financed by a grant from the Deutsche Forschungsgemeinschaft to K. Schmidt-Koenig (Univ. Tfibingen).

Appendix 1

443

Plant family and species No Part Neutral Acid Hemi- Soluble Total Extract. detergent detergent cellulose sugar protein protein fiber fiber

Condensed Alkaloid tannin

Chemical composition of leaves eaten by Avahi l. laniger at Andasib6

Annonaceae Artabotrys sp. 311 yl 63.5

Erythroxylaceae Erythroxylon buxifolium 330 ml 64.0 49.0 15.0

330 yl 85.5 350 yl 77.7 52.7 25.0

E. sp. 369 ml 60.5 47.0 13.5 240 yl 60.2

Euphorbiaceae Antidesma petiolare 238 1 63.5

413 yl 43.9 24.8 19.1 Uapaca densifolia 332 yl 66.7

Guttiferaceae Garcinia verrucosa 255 yl 51.3 42.4 8.9

Hypericaceae Haronga madagascariensis 362 ml 48.3 47.2 1.1

362 yl 49.3 59.2 0 Zauraceae

Ocotea sp. 244 yl 69.9 Ravensara coriacea 405 yl 75.8 44.9 30.9 R. ovalifolia 317 yl 57.6

Melastomataceae Dichaetantera oblongifolia 333 yl 50.9 Memecylon sp. 305 yl 81.1

313 yl 67.0 Moraceae

Pachytrophe dimepate 354 yl 67.4 55.8 11.6 Myrsinaceae

Oncostemum palmatiforme 382 yl 48.7 O. sp. 409 yl 54.7

Myrtaceae Eugenia sp. 312 yl

Ochnaceae Campylospermum anceps 351 yl 67.1 49.0 18.1

Pittosporaceae Pittosporum polyspermum 331 yl 54.5

Rhizophoraceae Carallia brachyata 254 ml 68.3 37.8 30.4

254 yl 62.2 33.5 28.8 Rubiaceae

Canthium sp.

Gaertnera sp. Sapindaceae

Allophyllus cobbe arboreus Plagioscyphus jumellei

Not identified

Chemical composition of leaves

A eanthaeeae Mendoncia sp.

Cunoniaceae Weinmannia rutenbergii

Euphorbiaceae Blotia madagascariensis Lautenbergia sp. Suregada laurina

217 ml 62.8 43.7 19.0 217 yl 69.6 44.2 25.4 242 yl 400 yl 71.0 55.0 16.0

393 yl 76.4 314 ml 63.5 314 yl 56.5

304 yl 75.9 309 1 40.8 419 yl 54.0

eaten by

52.8 10.7 ~ . 8 11.7

48.7 5.3

Cheirogaleus major at Andasib6

252 ml 76.4

402 yl 76.0

418 yl 56.7 374 yl 42.7 387 yl 68.6 44.0 24.6

10.7

12.9 2.2 3.2

11.5 15.8

11.2 5.5

10.2

15.7

11.9 4.2

10.0 5.4

16.6

4.0 2.0 8.2

10.0

8.1 7.2

13.0

14.9 11.2

19.3

20.1

9.5 7.0

26.9

8.3

7.7

6.0 8.4

10.7 5.5 8.8

3.5 9.1

13.8

18.1

9.5 7.0

8.9 7.3

11.2

5.6 15.0

7.0

4.1

13.4 12.8

35.6

26.2 5.0

14.0 38.2 30.6

46.6 14.2 26.2

13.1

21.8 10.3

26.5 11.0 64.3

5.6 4.1

27.5

16.4

39.4 17.5

7.7 16.7 7.3 33.9

7.1 3.9 4.5

12.1 29.1 9.8 68.6 7.9 29.2 11.3 27.7

3.4 17.9 7.8 25.0 6.5 23.2 8.0 51.4

11.7 16.4 8.7 34.2

3.2 12.1 5.5 9.1 10.6 7.2 31.5

10.3 13.2 8.9 29.8

2.6 13.0 2.9 8.1 4.8 9.4 7.4 10.9 10.9 13.8

i

m

n

m

m

I

4.3 0.4 3.0 --

7.3 7.2 18.3 +

13.0 6.8 0 -- 8.4 3.6 5.8 -- 3.1 14.6 0 2.3 +

444

Appendix 1 (continued)



Flacourtiaceae Aphloia theaeformis Ludia mad/sis L. scolopioides

Guttiferaceae Ochrocarpos orthocladus Rheedia sp. Symphonia louvelli

Moraceae Ficus pyrifolia

Myrsinaceae Oncostemum sp.

Myrtaceae Eugenia sp.

Papillonaceae Dalbergia baroni

eoaceae Bambusa sp.

Rosaceae Rubus mollucana Prunus persica

Rubiaceae Enterospermum resinosum Rhotmannia taolanana Trycalinia sp.

Chemical composition of leaves

Moraceae Ficus pyrifolia F. soroceoides

eoaceae

315 yl 41.4 13.8 6.5 379 yl 269 yl 67.7 7.1 1.3

410 yl 50.2 7.6 15.1 372 yl 375 yl 74.4 65.0 9.4 8.3 15.8 13.4

404 yl 64.4 27.1 37.4 3.6 28.2 3.5

382 yl 48.7 8.1 13.4

256 yl 72.2 4.7 9.6

265 yl 65.5 8.3 10.7

427 yl 87.1 36.5 50.6 23.5 37.7 2.3

318 ys 73.9 3.3 3.5 343 yl 46.7 10.5 2.1

201 yl 53.4 9.9 9.6 373 yl 381 yl 61.2 4.2 7.7

eaten by Hapalemur griseus at Andasib6

20.9

17.1

4,0

52.4

6.4

39.4

14.8

68.7

0

11.1 6.2

59.0

16.5

404 yl 64.4 27.1 37.3 3.6 28.2 3.5 6.4 345 ml 62.8 36.1 26.7 6,1 17.3 1.0 8.7

Bambusa sp. 421 yp 47.1 16.6 30.6 12,1 27.3 7.9 422 mp 52.9 22.2 30.8 13.4 24.6 5.1 423 lb 84.8 30.7 54.1 9.7 41.3 3.1 425 ys 78.9 36.3 42.5 11.5 31.6 2.7 427 yl 87.1 36.5 50.6 5.2 37.7 2.3

Cephalostachium sp. 426 yl 77.9 36.5 41.3 23.5 32.1 4.1

Chemical composition of leaves eaten by Indri indri at Andasib6

Acanthaeeae Mendoncia sp. 334 yl 54.3 4.6 5.3

Anaeardiaceae Protorhus ditimena 245 yl 44.6 19.6 10.1 P. thouvenotii 222 yl 66.0 49.9 16.1 7.8 16.8 9.0

Annonaceae Xylopia flexiosa 368 yl 82.3 3.7 5.5

Apocynaceae Carissa edulis 370 ml 63.5 10.0 5.4

Araliaceae Scheffiera voantsilana 230 yl 47.4 50.4 0 8.5 2.9 2.0

Erythroxylaceae Erythroxylon buxifolium 247 yl 63.5 42.2 21.3 13.4 18.2 6.2 E. sp. 369 yl 61.7 50.4 11.3 13.5 10,6 6.7 E. sp. 385 yl 64.9 14.1 9.9

Euphorbiaceae Blotia mad/sis 259 yl 74.5 53.5 21.0 5.5 17,9 6.2 B. oblongifolia 364 yl 80.2 60.7 19.5 4.2 14.3 3.8

Guttif eraceae Calophyllum milvum 243 yl 51.1 , 36.7 14.4 10.1 14.5 8.1 C. sp. 232 yl 48.6 37.5 11.1 14.3 17.7 13.9 Ochrocarpos mad/sis 377 yl 34.2 19.2 15.0 3.0 17.1 10.8 Symphonia louvelii 375 yl 74.4 65.0 9.4 8.3 15.8 13.4 S. passiculata 231 yl 45.8 10.6 15.0

2.4 2.4 3.5 2.3 0 2.2

26.1

61.2 60.8

30.8

42.9

13.5

56.8 30.5 37.8

17.8 15.9

80.6 32.6 0

52.4 20.4

m

m

+

+ +

w

+

445


Plant family and species No Part Neutral detergent fiber

Acid detergent fiber

Hemi- cellulose

Soluble sugar

Total protein

Extract. protein


Lauraceae Ocotea similis O. sp.

Ravensara helicina R. ovalifolia

376 yl 244 ml 244 yl 250 1 236 1 317 yl

69.8 69.9 64.8 68.4 57.6

Loganiaceae Anthocleista mad/sis 248 yl 47.4

Myrtaceae Eugenia gavoala 324 yl 76.0 E. rotramena 326 yl 58.3 51.1 E. sp. 233 1 57.6 E. sp. 246 yl 32.4 E. sp. 260 yl 84.1 E. sp. 328 yl 83.0 E. sp. 366 yl 47.9

Rhizophoraceae Carallia brachyata 249 yl 62.6

Sapindaceae Tinopsis apiculata 327 ml 83.6

327 yl 87.8 307 yl 80.2

Chemical composition of leaves eaten by Lemurf. fulvus at Andasib6

Acanthaeeae Mendoncia sp. 334 yl 54.3

Annonaceae Xylopia buxifolia 257 yl 54.9 45.3

258 yl 42.8 Apocynaceae

Carissa edulis 339 yl Aquifoliaceae

Ilex mitis 268 yl 39.4 Apaliaceae

Polyscias oligocias 341 yl 47.8 Chlaenaceae

Rhodolaena bakeriana 261 yl 65.5 Cunoniaceae

Weinmannia bojeriana 266 yl 57.0 Ebenaceae

Diospyros sp. 360 yl Erythroxylaceae

Erythroxylon buxifolium 350 yl 77.8 52.7 E. sphaeantum 335 yl -

Euphorbiaceae Blotia mad/sis 418 yl 56.7 Suregada laurina 336 yl 42.6

337 yl Flacourtiaceae

Aphloia theaeformis 315 yl 41.1 Ludia ludiaefolia 349 yl 62.5

Lauraceae Revensara ovalifolia 317 yl 57.6

Melastomataceae Dichaetantera oblongifolia 333 yl 50.9 Memecylon sp. 417 yl

Monimaceae Dycaryopsis capuronii 264 yl 72.8

Myrisinaeceae Oncostemum sp. 409 yl 54.7 O. sp. 340 yl O. sp. 342 yl 39.0

7.2

9.7

25.2

1.9 9.1

10.0 14.2

8.4 16.6

9.5

2.7 2.6 5.4 6.1 2.3 3.5 5.0

8.8

3.7 3.0 2.5

4.6

6.0 10.3

9.3

8.7

2.4

4.4

3.2 6.6

13.0 13.3

13.8 11.9

16.6

4.0

7.2

7.2

17.9

5.4

14.9

25.6

7.1 9.5 8.9 9.3 8,1

11,2

4.8

8.3 4.7 5.0 7.5

14.1 11.9 5.2

10.2

5.2 6.8 6.0

5.3

12.3 8.3

3.1

3,8

13.9

3.0

10.7 15.5

6.8 3.5

6.5 7.1

11.2

5.6

7.0

12.8

5.8

6.9 17.7 26.5 77.1 54.7 64.3

5.4

6.3 6.6

17.0 15.1

5.9 20.6 14.7

34,8

8.4 5.9 2,7

26.1

42.8 65.0

1.0

14.8

14.2

20.4

14.0 37.8

0 3.4

20.9 9.9

64.3

5.6

75.0

17.5

25.5

+

p

+ +

+

+ +




Myrtaceae Eugenia emyrnesis 262 yl 73.2 E. sp. 251 yl 58.3

Ochnaceae Campylospermum anceps 351 yl 67.1

Oleaceae Noronhia sp. 408 yl

Rhizophoraceae Carallia brachyata 356 yl 69.7

Rubiaceae Danais sp. 263 yl 60.0

Rutaceae Evodia densifolia 358 yl 77.2

Sapindaceae

2.1 6.4 7.8 2.9 14.9 4.8

49.0 18.1 7.7 16.7 7.3 33.9

Beguea apetala 408 yl

Chemical composit ion of leaves eaten by Lepilemur m. mustelinus at Andasib6

15.9 7.4 62.7

8.7 0.1 0

3.6 16.0 13.3

m

m

Annonaceae Xylopia buxifolia 257 yl 54.9 45.3 9.7 6.0 14.9 12.3 42.8 +

Araliaceae Polyscias sp. 411 1 + Polyscias sp. 416 1 +

Capparidaceae Crataeva sp. 389 yl 43.9 4.2 2.0 3.2 +

Dichapetalaceae Dichapetalum lecosei 278 1 71.8 1.8 0 31.9 -

Erythroxylaceae Erythroxylon sp. 277 1 79.9 9.8 6.0 56.4 -

Euphorbiaceae Antidesma petiolare 234 ml 61.0 9.0 8.2 18.6 + Blotia oblongifolia 235 yl 80.7 60.4 20.4 3.7 14.0 2.8 12.6 -

390 ml 83.4 55.2 28.3 4.6 20.3 2.8 11.4 + 390 yl 84.9 62.5 22.4 4.0 14.8 2.0 16.7 +

Cleistantinopsis sp. 301 ml 63.2 4.9 4.3 19.2 - 302 ml 57.0 44.4 12.7 6.4 11.2 6.1 31.5 -

Lautenbergia multispicata 241 ml 60.0 5.4 3.8 11.5 + Suregada laurina 387 yl 68.6 44,0 24.6 3.1 14.6 0 2,3 +

Flacourtiaceae Aphloia theaeformis 300 ml 52.4 40.6 11.8 10.0 12.1 7.8 19.9 -

Guttiferaceae Garcinia verrucosa 255 yl 51.3 7.5 1.1 3.0 -

Jaeinaeeae Leptolus citroides 297 1 51.3 7.5 1.1 3.0 -

Zauraceae Ocotea laevis 414 yl 66.9 40.7 26.2 2.6 26.5 10.6 4.2 +

Lecythidaeeae Foetidia asymmetrica 395 yl 50.5 36.5 14.0 6,5 14.6 8.5 28.8 -

Melastomataceae Memecylon sp, 396 yl 53.6 50.2 3.4 1.7 2.2 2.2 0.8 -

Mimosaceae Dichrostachys sp. 374 yl 42.7 8.4 3.6 5.8 -

Myrsinaeeae Oncostemum sp. 409 yl 54.7 7.2 12.8 17.5 -

Myrtaeeae Eugenia rot ramena 276 1 85.2 7.6 8.9 13,9 -

Rubiaeeae Canthium sp. 415 yl 43.5 28.2 15.3 4.5 12.1 5.0 2.0 + Craterispermum sp, 412 yl 50.6 34.2 16.5 3.1 9,5 1.4 1.3 +

Sapindaeeae Neotina coursii 253 yl 65.8 48.2 17.6 5.0 17,9 8.9 16.7 -

Violaceae Rinorea buUata 3.91 yl 60.2 1.9 8,0 2.2 -

No - reference number of plant collection. Specimens are stored at the Parc Tsimbazaza, Tananarive, Madagascar. yl young leaf, ml mature leaf, I leaf of unknown age, lb leaf base, ys young shoot, yp/mp pitch of young or mature stems of bamboo. Except for condensed tannins and alkaloids values are percentages of dry weight. Condensed tannins are in relative units as equivalents of quebracho tannin. Alkaloids are indicated as present or absent. Plants have been analysed by Jean-Prosp~re Abraham, Andasib6, Madagascar

447

A p p e n d i x 2

Plant family and species Lemur species Extractable protein Soluble sugar Condensed tannin Alka- loids

Chemical composition of fruits eaten by different lemur species at Andasib6

Ebenaceae Diospyros sp. Cm 7.3 8.9 11.0 -

Euphorbiaceae Drypetes mad/sis Mr 5.5 8.5 2.8 -

Flacourtiaceae Aphloia theaeformis (unripe) Cm 6.8 12.5 48.0 - Ludia scolopeoides Lf + Scolopia sp. Cm 7.4 20.4 54.8 +

Guttiferaceae Calophyllum milvum Lf 5.5 11.6 42.2 - Garcinia verrucosa Ii, Lf, Mr Rheedia sp. A1, Lf, Mr 11.2 2.8 7.9 - Symphonia louvelii Lf S. tanalensis Ii, Lf S. sp. I Lf 7.2 12.8 27.2 + S. sp. II Ii, Lf 8.3 16.l 41.8 -

Hypericaceae Psorospermurn sp. Lm, Mr

Hyrsinaceae Oncostemum sp. Mr

Lauraceae Cryptocarya thouvenotii Cm Ocotea cymosa Cm, Lf 5.9 5.2 3.8 + Ravensara flavescens Ii, Lf R. pervillei Ii

Loganiaceae Anthocleista rhizophora Cm 4.1 3.4 2.8 +

Melastomataceae Clidemia hirta Hg, Lf, Mr 6.8 11.8 2.3 - Medinilla sp. Mr 3.8 11.7 1.0 - Memecylon sp. Mr 11.6 2.0 2.2 -

Moraceae Ficus pachyclada Lf 2.9 25.0 31.4 - F. soroceoides Cm, Lf 2.1 12.6 28.0 +

Myrtaceae Eugenia emyrnensis Cm, Lf, Lm 5.7 20.0 31.4 - E. sp. Lf 11.2 9.2 3.5 -

Rubiaeeae Canthium sp. I Lf, Mr 10.8 7.9 2.5 - C. sp. II Lm 0 6.5 30.1 - Gaertnera sp. Cm 2.9 15.9 29.8 -

Sapindaceae Tinopsis apiculata Cm, Ii, Lf 11.8 4.1 17.4 -

Sapotaceae Gambeya boiviniana A1, Ii, Lf 13.0 @6 9.8 +

Vacciniaceae Vaccinium emynasea Cm 4.5 7.5 20.2 -

Verbenaceae Lantana camarra Cm, Mr 3.4 10.4 0 - Vitex pachyclada Lf 3.1 12.8 38.7 -

Not identified Lf 5.1 21.0 23.3 -

A1 = Avahi l. laniger ; Cm = Cheirogaleus major; Hg = Hapalemur griseus ; Ii =- Indri indri ; Lf= Lemur f fulvus ; Lm = Lepilemur m. mustelinus ; Mr = Microeebus rufus

448

Appendix 3



Chemical composition of leaves eaten by Avahi l. occidentalis at Ampijoroa

Anacardiaceae Protorhus sp. 516 yl 68.1 57.1 11.5 4.6

Celastraceae Mystroxylon aethiopicum 579 1

Erythroxylaceae Erythroxylum sp. 568 1 58.5 35.5 23.0 11.1

Meliaceae Astrotrichilia asterotricha 559 ml 59.4 48.3 11.1 14.9 Cedrelopsis sp. 526 ml 46.6 31.5 15.1 11.2 Neobeguea vahilava 578 1 74.8 73.0 1.8 2.8

Oleaceae Ancolosa pervillei 520 yl 61.8

Rubiaceae Tarenna homollida 580 1 63.4 42.7 20.7 5.0

Sapo taceae Capurodendron 574 yl 68.1 43.6 24.5 4.4 rubrocostatum

Sterculiaceae Nesogordonia normandii 523 1 70.0 20.9 49.1 12.0

Not identified 560 1 62.3 53.0 9.3 3.4

Chemical composition of leaves eaten by Lepilemur m. edwardsi at Ampijoroa

Apocynaceae Pandaca debrayi 577 1 34.8 21.0 13.8 8.2

Celastraceae Mystroxylon aethiopicum 571 yl 67.9 55.4 12.5 5.4

571 ml 60.0 47.5 12.6 6.4 Erythroxylaceae

Erythroxylum sp. 568 1 58.5 35.5 23.0 11.1 Euphorbiaceae

Drypetes sp. 508 1 70.3 47.0 23.3 5.6 517 1 71.7 44.8 26.9 8.7

Ochnaceae Diporidium ciliatum 576 1 72.3 47.0 25.3 6.2

Oleaceae Noronhia sp. 521 1 68.0 35.3 32.7 9.9

Papillonaceae Dalbergia greveana 562 1 55.9 32.2 23.7 8.3

Rubiaceae Gardenia sp. 1

Sapindaceae Macphersonia gracilis 507 1 62.6 42.6 19.9 4.5

Sterucliaceae Not identified 572 1 73,7 62.5 11.2 4.5

Verbenaceae Vitex bojeri 561 1 70.3 44.6 25,7 3.5

Not idenified 569 1 19.8 13.0

9.1 4.8 9.5

25.8 12.5 56.0

14.5 10.7 77.5 18.8 11.8 67.0 9.5 9.5 5.0

6.6

15.5 4.0 2.5

21.9 7.4 21.5

44.8 10.5 3.2

13.1 10.7 27.0 m

7.8 1.8 2.0 +

9.0 4.1 5.5 -- 8.5 3.5 12.0 -

25.8 12.5 56.9 -

18.7 5.2 29.5 -- 22.1 5.6 37.0 --

23.6 8.5 28.5 --

22.2 1.1 4.5 +

20.5 6.6 17.5 +

+

16.1 5.2 3.5 --

7.2 3.3 22.5 --

19.4 3.9 5.2 +

2.7 7.8 --

For explanations see Appendix 1

References

Bourli~re F (1985) Primate communities: Their structure and role in tropical ecosystems. Int J Primatol 6:1-26

Bradford M (1976) A rapid and sensitive method for the quantifica- tion of microgram quantities of protein utilizing the principle of protein-dye-binding. Anal Biochem 72:248-254

Brattsten LB (1979) Biochemical defense mechanisms in herbivores against plant allelochemicals. In: Rosenthal GA, Janzen DH (eds) Herbivores. Academic Press, London New York, pp 200- 270

Chapman RF, Blaney WM (1979) How animals perceive secondary compounds. In: Rosenthal GA, Janzen DH (eds) Herbivores. Academic Press, London New York, pp 161-168

Charles-Dominique P, Cooper HM, Hladik A, Hladik CM, Pages E, Pariente GF, Petter-Rousseaux A, Petter JJ, Schilling A (1980) Nocturnal Malagasy primates. Academic Press, New York

Chivers D J, Hladik CM (1980) Morphology of the gastrointestinal tract in primates: comparison with other mammals in relation to diet. J Morphology 166:337-386

Clutton-Brock TH, Harvey PH (1977) Primate ecology and social organisation. J Zool, London 183:1-39

449

Cody ML (i 974) Competition and the structure of bird communities. Princeton Univ Press, Princeton

Cromwell BT (1955) The alkaloids. In: Paech K, Tracy MV (eds) Modern methods of plant analysis. 4, pp 367-374

Deichsel G, Trampisch HJ (1985) Biometry: Clusteranalyse und Diskriminanzanalyse. G Fischer, Stuttgart

Dewar RE (1984) Recent extinctions in Madagascar: The loss of the subfossil fauna. In: Martin PS, Klein RG (eds) Quaternary Extinctions. Univ Arizona Press, Phoenix, pp 574-593

Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 18:586-608

Eze JMO, Dumbroff EB (1982) A comparison of the Bradford and Lowry methods for the analysis of protein in chlorophyl- lous tissue. Can J Bot 60:1046-1049

Ganzhorn JU (1987a) Soil consumption in two groups of semi-free ranging lemurs (Lemur catta and Lemur fulvus). Ethology 74:146-154

Ganzhorn JU (1987b) A possible role of plantations for primate conservation in Madagascar. Am J Primatol 12:205-215

Ganzhorn JU (1988) Primate species separation in relation to secondary plant chemicals. In: Rumpler Y, Preuschoft HG (eds) Speciation systematics and conservation of Prosimians (in press)

Ganzhorn JU, Rabesoa J (1986) The aye-aye (Daubentonia mada- gaseariensis) found in the eastern rainforest of Madagascar. Folia Primatol 46:125-126

Gause GF (1969) The struggle for existence. Hafner Publ Comp, New York

Glander KE (1982) The impact of plant secondary compounds on primate feeding behavior. Yearbook Phys Anthropol 25:1-18

Glaser D (1986) Geschmacksforschung bei Primaten. Vierteljah- resschrift der Naturforschenden Gesellschaft in Zfirich 131:92-110

Glaser D, Hobi G (1985) Taste responses in primates to citirc and acetic acid. Int J Primatol 6 : 395-398

Goering HK, van Soest PJ (1970) Forage fiber analysis. Agric Handb No 379. Agricultural Research Service. US Department of Agriculture

Harrington JE (1975) Field observations of social behavior of Le- mur fulvus fulvus E. Geoffroy 1812. In: Tattersall I, Sussman RW (eds) Lemur biology. Plenum Press, New York, pp 259- 279

Hladik CM (1977) A comparative study of the feeding strategies of two sympatric species of leaf monkeys : Presbytis senex and P. entellus. In: Clutton-Brock TH (ed) Primate ecology: studies of feeding and ranging behaviour in lemurs monkeys and apes. Acad Press, London, pp 324-353

Hladik CM (1979) Diet and ecology of Prosimians. In: Doyle GA, Martin RD (eds) The study of Prosimian behaviour. Academic Press, New York, pp 307-357

Hladik CM, Hladik A, Bousset J, Valdebouze P, Viroben G, De- lort-Laval J (1971) Le rrgime alimentaire des primates de l'Ile de Barro-Colorado (Panama). Rrsultats des analyses quantita- tires. Folia Prirnatol 16:85-122

Hutchinson GE (1957) Concluding remarks. Cold Spring Harbor Syrup Quant Biol 22: 415-427

Janzen DH, Waterman PG (1984) A seasonal census of phenolic, fiber and alkaloids in foliage of forest trees in Costa Rica: Some factors influencing their distribution and relation to host selection by Sphingidae and Saturniidae. Biol J Linn Soc 21 : 439-454

Kates M (1972) Techniques of lipidology. In: Work TS, Work E (eds) Laboratory techniques in biochemistry and molecular biology, vol 3 North-Holland Publ Comp Amsterdam, pp 267- 610

Martin JS, Martin MM (1982) Tannin assays in ecological studies: lack of correlation between phenolics, proanthocyanidins and protein-precipitating constituents of mature foliage of six oak species. Oecologia (Berlin) 54: 205-211

Martin RD (1972) Behaviour and ecology of nocturnal Prosimians. Z Tierpsychol Beiheft 9:43-89

McNaughton SJ, Georgiadis NJ (1986) Ecology of African gazing and browsing mammals. Ann Rev Ecol Syst 17:39-65

Mittermeier RA, Oates JF (1985) Primate diversity: The world's top countries. Prim Conserv 5:41-48

Mole S, Waterman PG (1987a) A critical analysis of techniques for measuring tannins in ecological studies. I. Techniques for chemically defining tannins. Oecologia (Berlin) 72:137-147

Mole S, Waterman PG (1987b) A critical analysis of techniques for measuring tannins in ecological studies. II. Techniques for biochemically defining tannins. Oecologia (Berlin) 72:148- 156

Miihlenberg M (1976) Freilandrkologie. Quelle und Meyer, Hei- delberg

Oates JF, Swain T, Zantovska J (1977) Secondary compounds and food selection by Colobus monkeys. Biochem Syst Ecol 5:317-321

Petter JJ, Peyrieras A (1970) Nouvelle contribution ~ l'~tude d'un l~murien malgache, le aye-aye (Daubentonia madagascariensis). Mammalia 34:167-193

Pollock JI (1975 a) The social behaviour and ecology of Indri indri. Unpubl Ph D thesis. London Univ

Pollock JI (1975 b) Field observation on Indri indri: A preliminary Report. In: Tattersall I, Sussman RW (eds) Lemur Biology. Plenum Press, New York, pp 287-311

Pollock JI (1979) Spatial distribution and ranging behavior in Le- murs. In: Doyle GA, Martin RD (eds) Academic Press, New York, pp 359-409

Pollock JI (1986) A note on the ecology and behavior of Hapalemur griseus. Prim Conserv 7:97-101

Pollock JI, Constable ID, Mittermeier RA, Ratsirarson J, Simons H (1985) A note on the diet and feeding behavior of the Aye- aye, Daubentonia madagascariensis. Int J Primatol 6:435-447

Rhoades DF (1985) Offensive-defensive interactions between herbivores and plants: their relevance in herbivore poluation dynam- ics and ecological theory. Am Nat 125:205-238

Richard AF (1978) Behavioral variation. Bucknell Univ Press Richard AF (1985) Primates in nature. Freeman and Co, New

York Robbins CT (1983) Wildlife feeding and nutrition. Academic Press,

New York Roosmalen MGM van (1984) Subcategorizing food in primates.

In: Chivers D J, Wood BA, Bilsborough A (eds) Food acquisition and processing in primates. Plenum Press, New York, pp 167-175

SAS/STAT (1985) Guide for Personal Computers. Cary Schaik CP van, Hooff JARAM van (1983) On the ultimate causes

of primate social systems. Behaviour 85: 91-117 Seligson D, Szalay FS (1978) Relationship between natural selec-

tion and dental morphology: tooth function and diet in Lepile- tour and Hapalemur. In: Butler PM, Joysey KA (eds) Develop- ment, Function and Evolution of Teeth. Academic Press, Lon- don, pp 28%307

Siegel S (1956) Nonparametric Statistics. McGraw-Hill Kogahusha Ltd, Tokyo

Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (1986) Primate Societies. Univ Chicago Press, Chicago

Sourd C, Gautier-Hion A (1986) Fruit selection by a forest guenon. J Anita Ecol 55 : 235-244

Tattersall I (1982) The primates of Madagascar. Columbia Univ Press, New York

Terborgh J (1983) Five New World Primates. Princeton Univ Press, New Jersey

Terborgh J (1986) Keystone plant resources in the tropical forest. In: Soul~ ME (ed) Conservation Biology. Sinauer, Sunderland, pp 330-344

Terborgh J, Janson CH (1986) The socioecology of primate groups. Ann Rev Ecol Syst 17:111-136

Waterman PG (1984) Food aquisition and processing as a function of plant chemistry. In: Chivers D J, Wood BA, Bilsborough A (eds) Food acquisition and processing in primates. Plenum Press, New York, pp 177-211

450

Wisdom CS, Gonzales-Coloma A, Rundel PW (1987) Ecological tannin assays. Oecologia (Berlin) 72:395-401

Wrangham RW (1980) An ecological model of female-bonded primate groups. Behaviour 75:262-300

Wright PC (1985) Costs and benefits of nocturnality of Aotus trivir- gatus (the night-monkey). Ph D thesis. City Univ New York

Wright PC (1986) Ecological correlates of monogamy in Aotus and Callicebus. In: Lee PC, Else J (eds) Primate ecology and conservation. Cambridge Univ Press, pp 159-167

Received November 11, 1987

food partitioning among malagasy primates

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